Lutzomyia longipalpis

Last updated

Lutzomyia longipalpis
Lutzomyia longipalpis-sandfly.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Diptera
Family: Psychodidae
Genus: Lutzomyia
Species:
L. longipalpis
Binomial name
Lutzomyia longipalpis
(Lutz & Neiva, 1912)

Lutzomyia longipalpis (L. longipalpis) is a species complex of sandfly belonging to the family Psychodidae. This species is primarily present in Central and South America, but has also appeared in Mexico. There have been reports of L. longipalpis as far south as Argentina, as they are found in a wide variety of ecological conditions. [1] Both males and females feed on sugars from plants and aphids, but only adult females feed on the blood of other mammals. The species has recently begun appearing in urban areas throughout Brazil, and serves as a key vessel for the propagation of the parasite Leishmania infantum . [1] The presence of these flies appears to be strongly correlated to the presence of domestic chickens in Latin America. The first major urban outbreak of the lethal Visceral leishmanias epidemic was detected in Teresina, Piauí State in the early 1980s following a massive planting of acacias. [2]

Contents

History of taxonomy

L. longipalpis has only recently (2017) been accepted as a complex of sibling species as opposed to a heterogeneous species. Earlier on, there were many doubts that L. longipalpis constituted a single species due to its wide geographic distribution over Latin America. Populations of L. longipalpis and sand flies studied within Brazil showed morphological differences. [3] Males in the northern region of Brazil had only one pair of pale tergal spots, while those in the northeastern region of Brazil had two pairs. Thus, it was hypothesized that the species might be further broken down into two different forms. [3] This hypothesis was confirmed through insemination experiments as males from one form of the species were unable to successfully mate with females of the other form. [4]

Since then, several studies within Brazil have been conducted to support the hypothesis that L. longipalpis is a species complex. Studies involving isoenzyme electrophoresis, genetic polymorphism assessments of DNA and mRNA, cytogenetics, analysis studies of nucleotide variation in the NADH dehydrogenase subunit 4, as well as assessments of other mitochondrial genes are all part of mounting evidence supporting the species complex hypothesis. [3] In 2001, Lutzomyia psudolongipalpis was characterised by María Dora Feliciangeli's research group as one of the species within the complex. Subsequent research has indicated that there may be 8 distinct species within the complex. [5]

Habitat

L. longipalpis is the most abundant species of sandfly occupying northeastern Brazil, representing 97.9% of all phlebotomine sand flies present there. This species is followed in descending order of abundance by L. evandroi, L. lenti, and L. sallesi. L. longipalpis. These flies are most prevalent near animal shelters, such as chicken coops and corrals. They can also be found in houses, but only in small quantities. [6]

Physiology

L. longipalpis possesses the enzyme Trypsin in their midgut, which is responsible for the primary digestion of proteins in females. Trypsin activity is naturally decreased by 36% to 46% during the first and second days after the second gonadotrophic cycle. [7] However, the presence of the Leishmania parasite within the sandfly is associated with even lower levels of activity of the protease enzyme. This modulation in Trypsin activity after a sandfly's second blood meal is suspected to produce a conducive physiological environment for Leishmania infections, which is exploited by the parasite. [8] Transmission and development of the disease are consequently dependent upon the sandfly's access to multiple blood meals. Dogs that have been treated with the LJM17 salivary protein from L. longipalpis presented a more powerful cellular immune response in response to infection. Higher levels of proinflammatory cytokines and chemokines were detected with a specific increase in the production of IFN-γ and IL-10, indicating a stronger and longer-lasting immune response to the disease antigen. The strong immune reaction in response to exposure to the salivary protein indicates the protein's potential use in the field as a treatment to vaccinate dogs who then become immune to the disease.

Midgut

The acidity of the sandfly midgut is maintained at a stable homeostatic pH level of ~6, even in the presence of strong buffer solutions. However, the proper digestion of blood requires an alkaline pH of 8.15 in the abdominal midgut for proteases like Trypsin to function properly. [9] Lutzomyia longipalpis females contain the ability to abruptly alter their physiology by switching the internal environment of the abdominal midgut from acidic to alkaline. The presence of undigested proteins serves as the acting stimulus to drive female sand flies to undergo a shift in abdominal midgut pH. Even though the pH of the abdominal midgut is alkaline, carbohydrate digestion is able to function efficiently due to the maintenance of the acidic pH of the thoracic midgut.

Diet

Humans are an important blood source for these flies, but they are also known to feed on dog, chicken, and armadillo blood. Blood from horses, guinea pigs, and humans provide the best nutrients to support L. longipalpis females in their reproduction processes. Interestingly, sand flies do not feed on the blood from cats or the opossums Monodelphis domestica . Most scientific evidence points towards L. longipalpis being eclectic feeders, signifying that they acquire blood from multiple sources. [10]

Dangers of Multiple Blood Meals

Although the feeding of blood is important for the maturation of oocytes, too many blood meals can also negatively impact the lifespan of females. Lutzomyia Longipalpis, like most other blood-sucking organisms, ingest large amounts of blood in a single meal. A female sandfly consumes between three and ten times its body weight in one feeding. [11] Blood is rich in proteins, consisting mainly of hemoglobin (Hb), which accounts for approximately 60% of the blood protein content. [11] The digestion of hemoglobin results in the release of high levels of the prosthetic group heme. Heme acts as a toxic molecule that can generate oxygen-reactive species and bypass membranes due to its high permeability. Elevated levels of heme in female L. longipalpis are suspected to be the cause of increased mortality for females that have ingested multiple blood meals. [11]

Pathogenesis

Leishmania infantum in a bone marrow smear. Leshmania infantum.JPG
Leishmania infantum in a bone marrow smear.

L. longipalpis plays a primary role in the transmission of Leishmania infantum throughout several countries in South America.This parasite directly causes visceral leishmaniasis, which is a severe disease that affects internal organs, including the spleen, liver, and bone marrow. The parasitic pathogen is transmitted through the bite of a sandfly, and although humans can be infected, humans cannot spread the disease further. Instead, domestic dogs are the primary amplification host for the parasite. [12]

Immune Response

The direct bite of an infected sandfly during blood feeding allows for the parasitic transmission of Visceral leishmaniasis from L. longipalpis to the vertebrate host. The sandfly saliva contains potent physiological compounds that cause anticoagulant, vasodilating, and anti-inflammatory activity, which influences the immune response of the host vertebrate. [13] Dogs that have been treated with the LJM17 salivary protein from L. longipalpis presented a more powerful cellular immune response in response to infection. Higher levels of proinflammatory cytokines and chemokines were detected with a specific increase in the production of IFN-γ and IL-10, indicating a stronger and longer-lasting immune response to the disease antigen. [13] The strong immune reaction in response to exposure to the salivary protein indicates the protein's potential use in the field as a treatment to vaccinate dogs who then become immune to the disease.

Microbiome of Midgut

For transmission of Leishmania to occur, it must first undergo development into an infective promastigote. This crucial step of development occurs in the midgut of Lutzomyia longipalpis. The microbiome of the midgut is a critical factor that influences the growth of the pathogen into its infective state. Sucrose-rich diets result in highly diverse, stable bacterial microbiomes. Meanwhile, blood-feeding diets cause a markable decrease in microbial richness, but this decrease is eventually corrected after a short period of time. Sandflies infected with Leishmania experience a progressive decline in the bacterial diversity of the midgut. Interestingly, the perturbation of the midgut microbiome due to the introduction of antibiotics causes the sand flies to become unable to support the parasitic growth of the pathogen. [9] This highlights the bacterial microbiome of the L. longipalpis midgut as another area of interest that can be explored to control the disease.

Interactions with domestic chicken

Latin American chicken. Orpington chicken head.jpg
Latin American chicken.

One study within Bahia, Brazil discovered that people with chicken coops in their homes were 4.21 times more likely to contract zoonotic visceral leishmaniasis (ZVL) compared to those who did not have chicken coops. However, other studies have not been able to verify this significant correlation. [12] Nevertheless, it is well known that L. longipalpis are highly abundant near chicken coops, but the relationship between chicken raising and ZVL is not fully understood because chickens are unable to harbor infections of the parasite. Although chickens cannot serve as host reservoirs for the disease, chickens may play a crucial role in sustaining populations of the sandfly vector for the disease, as well as attracting other mammals, such as dogs, for the parasite to potentially infect. [12]

Theories of Explanation

One factor possibly contributing to the high L. longipalpis presence near chickens is the feeding of sand flies on chicken blood. Chickens are dormant at night, which leave large areas of exposed skin susceptible to fly feeding. The epidermis of chickens is relatively thin (~0.02 mm), which allows the sandfly to more easily pierce the skin to acquire the blood nutrients. [12]

From an evolutionary standpoint, one theory proposes that male blood-sucking L. longipalpis may have gained a significant mating advantage by staying near chickens and waiting for females to arrive and feed. [12] At any given moment, the number of male flies far outweighs the number of female flies present on a chicken host, which is similar in size to their mating ritual of courtship. Thus, chickens may play a vital role as a hub for the propagation of the fly species. [12]

Another theory is that in general, many of these people who raise chickens in chicken coops tend to also raise other animals, such as pigs and livestock, in their yards. Dogs are commonly used as security to guard the chickens, which presents a convenient group of amplification hosts for the parasite within a concentrated area. [12]

Life History

Lutzomyia longipalpis larva. Lutzomyia longipalpis larva.jpg
Lutzomyia longipalpis larva.

The total developmental time for each generation lasts about 6–7 weeks. L. longipalpis follow a general life cycle common to sand flies consisting of eggs, larvae, and pupae, and winged adults. After the female acquires a blood meal, oviposition occurs within 5–9 days. After eggs are laid, they require 4–9 days to grow before they hatch. Larvae develop in 9–24 days, while pupae then develop in approximately 10 days. [14] Immature stages involve growth in the ground, and soil traps have identified chicken sheds as the optimal breeding site for L. longipalpis larvae. [15] Implications for the residence of these larvae suggest that larval control at chicken sheds could aid in control of adult flies and thus, disease pathogenesis with regards to L. infantum. [15]

Development

After emergence from pupae, both male and female L. longipalpis initially feed on sugars from plants and aphids, but as development occurs, only adult females are hematophagous. Both genders will consume sugar-rich foods, such as nectar, honey dew, and plant sap, but females will feed on a wide range of vertebrates, including dogs, chickens, horses, and humans. [16] The blood meal serves as an essential step for the maturation of the ovaries. After consuming a fulfilling amount of blood, the female starts its digestion, which requires three to four days. [16] Females are anautogenous insects, so egg development only occurs after a blood meal. Oviposition begins six days after the blood meal and generally lasts for six days. [17] However, a second blood feed is required to start a new cycle of digestion and oviposition. [18]

Mating

This species has an overall sex ratio of 2:1 for males to females, so males outnumber females. [6] Males of the species complex are attracted to vertebrate host odors called kairomones and collectively form nocturnal aggregations called leks near the hosts. Females, unlike males, are haematophagous and are attracted to the lek both by the kairomones secreted from the host, as well as the sex pheromones secreted by the males. [1]

Males

Males possess glands that secrete pheromones to attract females that can act over a distance of 240 cm. After birth, pheromone biosynthesis occurs after 12 hours, and it takes males 24 hours to become sexually mature. Male courtship behavior involves the aggregation of males who compete with one another by producing sex pheromones. [19] Males encircle females and use the vibrating movement and flapping of their wings to produce audible sounds. These pre-mating signaling frequencies resemble a song that the males use to attract and court the females. [3]

Ecology

Several abiotic factors, such as temperature, rainfall, and humidity have been shown to influence the population density size of these sand flies. Rainfall is the most influential variable accounting for population size as documented increases in population size occur during the rainy months and directly after the rainy period. [20] Higher relative humidity is significantly correlated with higher population sizes of the species, as well. [6]

Flora

Legume plant. Vetch (Vicia sp.) - Kitchener, Ontario 2018-07-14.jpg
Legume plant.

Because the diversity and quantity of plant wildlife are largely associated with the quality and availability of resources that insects can utilize, acacias have been targeted as a point of interest in their involvement with L. longipalpis and the propagation of its disease. [21] Acacia trees attract the presence of these sand flies due to their ability to provide protection from predators, allowing the flies to proliferate. Sand flies also require sugar from plants as their energy source. Plants from the family Fabaceae are preferentially selected for in the feeding diet of L. longipalpis, while other trees that may be more abundant, such as the Anacardiacea and Meliaceae families are not preferred by the fly species. [2] The Fabaceae family is commonly known as legumes and contain a mixture of carbohydrates ranging from simple sugars to complex heteropolysaccharides. The sandfly species are attracted to the specific carbohydrate composition of this plant species over others.

Related Research Articles

<i>Leishmania</i> Genus of parasitic flagellate protist

Leishmania is a parasitic protozoan, a single-celled organism of the genus Leishmania that is responsible for the disease leishmaniasis. They are spread by sandflies of the genus Phlebotomus in the Old World, and of the genus Lutzomyia in the New World. At least 93 sandfly species are proven or probable vectors worldwide. Their primary hosts are vertebrates; Leishmania commonly infects hyraxes, canids, rodents, and humans.

<span class="mw-page-title-main">Leishmaniasis</span> Disease caused by parasites of the Leishmania type

Leishmaniasis is a wide array of clinical manifestations caused by parasites of the Trypanosomatida genus Leishmania. It is generally spread through the bite of phlebotomine sandflies, Phlebotomus and Lutzomyia, and occurs most frequently in the tropics and sub-tropics of Africa, Asia, the Americas, and southern Europe. The disease can present in three main ways: cutaneous, mucocutaneous, or visceral. The cutaneous form presents with skin ulcers, while the mucocutaneous form presents with ulcers of the skin, mouth, and nose. The visceral form starts with skin ulcers and later presents with fever, low red blood cell count, and enlarged spleen and liver.

<span class="mw-page-title-main">Sandfly</span> Name of several types of blood-sucking fly

Sandfly or sand fly is a colloquial name for any species or genus of flying, biting, blood-sucking dipteran (fly) encountered in sandy areas. In the United States, sandfly may refer to certain horse flies that are also known as "greenheads", or to members of the family Ceratopogonidae. The bites usually result in a small, intensely itchy bump or welt, the strength of which intensifies over a period of 5-7 days before dissipating. Moderate relief is achieved with varying success through the application of over the counter products such as Benadryl (ingested) or an analgesic cream such as After Bite. Outside the United States, sandfly may refer to members of the subfamily Phlebotominae within the Psychodidae. Biting midges (Ceratopogonidae) are sometimes called sandflies or no-see-ums. New Zealand sandflies are in the genus of sand fly Austrosimulium, a type of black fly.

<i>Lutzomyia</i> Genus of flies

Lutzomyia is a genus of phlebotomine sand flies consisting of nearly 400 species, at least 33 of which have medical importance as vectors of human disease. Species of the genus Lutzomyia are found only in the New World, distributed in southern areas of the Nearctic and throughout the Neotropical realm. Lutzomyia is one of the two genera of the subfamily Phlebotominae to transmit the Leishmania parasite, with the other being Phlebotomus, found only in the Old World. Lutzomyia sand flies also serve as vectors for the bacterial Carrion's disease and a number of arboviruses.

<i>Phlebotomus</i> Genus of flies

Phlebotomus is a genus of "sand flies" in the Diptera family Psychodidae. In the past, they have sometimes been considered to belong in a separate family, Phlebotomidae, but this alternative classification has not gained wide acceptance.

<span class="mw-page-title-main">Cutaneous leishmaniasis</span> Medical condition

Cutaneous leishmaniasis is the most common form of leishmaniasis affecting humans. It is a skin infection caused by a single-celled parasite that is transmitted by the bite of a phlebotomine sand fly. There are about thirty species of Leishmania that may cause cutaneous leishmaniasis.

<span class="mw-page-title-main">Visceral leishmaniasis</span> Human disease caused by protist parasites

Visceral leishmaniasis (VL), also known as kala-azar or "black fever", is the most severe form of leishmaniasis and, without proper diagnosis and treatment, is associated with high fatality. Leishmaniasis is a disease caused by protozoan parasites of the genus Leishmania.

<span class="mw-page-title-main">Phlebotominae</span> Subfamily of flies

The Phlebotominae are a subfamily of the family Psychodidae. In several countries, their common name is sandfly, but that name is also applied to other flies. The Phlebotominae include many genera of blood-feeding (hematophagous) flies, including the primary vectors of leishmaniasis, bartonellosis and pappataci fever. In the New World, leishmaniasis is spread by sand flies in the genus Lutzomyia, which commonly live in caves, where their main hosts are bats. In the Old World, sand flies in the genus Phlebotomus spread leishmaniasis.

A canine vector-borne disease (CVBD) is one of "a group of globally distributed and rapidly spreading illnesses that are caused by a range of pathogens transmitted by arthropods including ticks, fleas, mosquitoes and phlebotomine sandflies." CVBDs are important in the fields of veterinary medicine, animal welfare, and public health. Some CVBDs are of zoonotic concern.

<i>Leishmania infantum</i> Species of parasitic protist

Leishmania infantum is the causative agent of infantile visceral leishmaniasis in the Mediterranean region and in Latin America, where it has been called Leishmania chagasi. It is also an unusual cause of cutaneous leishmaniasis, which is normally caused by specific lineages. Wild canids and domestic dogs are the natural reservoir of this organism. The sandfly species Lutzomyia longipalpis serves as the primary vector for the transmission of the disease.

<span class="mw-page-title-main">Canine leishmaniasis</span> Disease affecting dogs

Canine leishmaniasis (LEESH-ma-NIGH-ah-sis) is a zoonotic disease caused by Leishmania parasites transmitted by the bite of an infected phlebotomine sandfly. Canine leishmaniasis was first identified in Europe in 1903, and in 1940, 40% of all dogs in Rome were determined to be positive for leishmaniasis. Traditionally thought of as a disease only found near the Mediterranean basin, 2008 research claims new findings are evidence that canine leishmaniasis is currently expanding in continental climate areas of northwestern Italy, far from the recognized disease-endemic areas along the Mediterranean coasts. Cases of leishmaniasis began appearing in North America in 2000, and, as of 2008, Leishmania-positive foxhounds have been reported in 22 U.S. states and two Canadian provinces.

<i>Leishmania donovani</i> Species of intracellular parasite

Leishmania donovani is a species of intracellular parasites belonging to the genus Leishmania, a group of haemoflagellate kinetoplastids that cause the disease leishmaniasis. It is a human blood parasite responsible for visceral leishmaniasis or kala-azar, the most severe form of leishmaniasis. It infects the mononuclear phagocyte system including spleen, liver and bone marrow. Infection is transmitted by species of sandfly belonging to the genus Phlebotomus in Old World and Lutzomyia in New World. The species complex it represents is prevalent throughout tropical and temperate regions including Africa, China, India, Nepal, southern Europe, Russia and South America. The species complex is responsible for thousands of deaths every year and has spread to 88 countries, with 350 million people at constant risk of infection and 0.5 million new cases in a year.

<i>Leishmania tropica</i> Species of protozoan parasite

Leishmania tropica is a flagellate parasite and the cause of anthroponotic cutaneous leishmaniasis in humans. This parasite is restricted to Afro-Eurasia and is a common cause of infection in Afghanistan, Iran, Syria, Yemen, Algeria, Morocco, and northern India.

Leishmania braziliensis is a Leishmania species found in South America. It is associated with leishmaniasis.

Lutzomyia shannoni is a species of fly in the subfamily Phlebotominae, the phlebotomine sand flies. It is native to the Americas from the southeastern United States to northern Argentina. It has a disjunct distribution, and is only found in regions with suitable climates, habitat types, and host animals. It is well known as a vector of the vesicular stomatitis virus, which causes the disease vesicular stomatitis in animals, particularly livestock.

Lutzomia anthrophora is a species of what is commonly known as the sandfly in the order Diptera and it is a common vector for Leishmania mexicana.

<span class="mw-page-title-main">Maria Cristina Ferro</span> Colombian microbiologist (1947–2015)

Maria Cristina Ferro de Carrasquilla (1947–2015) was a Colombian microbiologist and Leishmaniasis researcher who worked for more than forty years at the National Health Institute of Colombia. Most of her research was focused on sandflies, which are Leishmaniasis vectors, contributing with the description of three new species: Lutzomyia torvida, Lutzomyia falcata, and Lutzomyia tolimensis. Given her research contributions, a sandfly species was named after her: Lutzomyia ferroae. Ferro also worked with Venezuelan equine encephalitis virus and received the Emeritus Researcher award from the National Health Institute of Colombia in 2007

Shaden Kamhawi a Jordanian scientist and the co-Editor-in-Chief of PLOS Neglected Tropical Diseases academic journal. She is a specialist in vector-borne diseases.

María Dora Feliciangeli was Professor of Medical Entomology at the University of Carabobo, Venezuela, who worked on the transmission of tropical parasites especially American trypanosomiasis and leishmaniasis. She was Coordinator of the National Reference Center of Sandflies and the Medical Entomology Section.

<i>Phlebotomus papatasi</i> Species of fly

Phlebotomus papatasi is a species of insects commonly known as sandflies. Due to their ectothermic climate limitations, P. papatasi are confined to regions with temperatures above sixty degrees Fahrenheit for at least three months of the year, spanning over much of the European Mediterranean, North Africa, the Middle East, and Central Asia. Around one thousand sandfly species have been described, belonging to the subfamily Phlebotominae within the family Psychodidae. The Psychodidae family belongs to the order Diptera within the class Insecta of the subphylum Hexapoda of the Arthropod phylum.

References

  1. 1 2 3 Spiegel, Carolina N.; Dias, Denise B. dos Santos; Araki, Alejandra S.; Hamilton, James G. C.; Brazil, Reginaldo P.; Jones, Théresa M. (14 November 2016). "The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication". Parasites & Vectors. 9 (1): 580. doi: 10.1186/s13071-016-1866-x . PMC   5109651 . PMID   27842601.
  2. 1 2 Lima, L., Mesquita, M., Skrip, L. et al. DNA barcode for the identification of the sand fly Lutzomyia longipalpis plant feeding preferences in a tropical urban environment. Sci Rep 6, 29742 (2016) doi : 10.1038/srep29742
  3. 1 2 3 4 Souza, Nataly A; Brazil, Reginaldo P; Araki, Alejandra S (2017). "The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex". Memórias do Instituto Oswaldo Cruz. 112 (3): 161–174. doi:10.1590/0074-02760160463. PMC   5319373 . PMID   28225906.
  4. ↑ Ward, Richard D.; Ribeiro, Armando L.; Ready, Paul D.; Murtagh, Angela; Ward, Richard D.; Ribeiro, Armando L.; Ready, Paul D.; Murtagh, Angela (1983). "Reproductive isolation between different forms of Lutzomyia longipalpis (Lutz & Neiva), (Diptera: Psychodidae), the vector of Leishmania donovani chagasi Cunha & Chagas and its significance to kala-azar distribution in South America". Memórias do Instituto Oswaldo Cruz. 78 (3): 269–280. doi: 10.1590/S0074-02761983000300005 .
  5. ↑ Contreras Gutierrez, María Angélica; HoyosLopez, Richard Onalbi; other co-authors, and five (2021). "DNA barcoding of Lutzomyia longipalpis species complex (Diptera: Psychodidae), suggests the existence of 8 candidate species". Acta Tropica. 221: 105983. doi:10.1016/j.actatropica.2021.105983. PMID   34048789 . Retrieved 7 April 2022.
  6. 1 2 3 Costa, Pietra Lemos; Dantas-Torres, Filipe; da Silva, Fernando José; Guimarães, Vanessa Cristina Fitipaldi Veloso; Gaudêncio, Kamila; Brandão-Filho, Sinval Pinto (May 2013). "Ecology of Lutzomyia longipalpis in an area of visceral leishmaniasis transmission in north-eastern Brazil". Acta Tropica. 126 (2): 99–102. doi: 10.1016/j.actatropica.2013.01.011 . PMID   23369878.
  7. ↑ E. L. Telleria, A. P. O. de Araújo, N. F. Secundino, C. M. d'Avila-Levy, and Y. M. Traub-Csekö, “Trypsin-like serine proteases in Lutzomyia longipalpis - expression, activity and possible modulation by Leishmania infantum chagasi,” PLoS ONE, vol. 5, no. 5, Article ID e10697, 2010.
  8. ↑ C. S. Moraes, K. Aguiar-Martins, S. G. Costa, P. A. Bates, R. J. Dillon, and F. A. Genta, “Second Blood Meal by Female Lutzomyia longipalpis: Enhancement by Oviposition and Its Effects on Digestion, Longevity, and Leishmania Infection,” BioMed Research International, vol. 2018, Article ID 2472508, 10 pages, 2018. doi : 10.1155/2018/2472508.
  9. 1 2 Kelly, Patrick H., et al. “The Gut Microbiome of the Vector Lutzomyia Longipalpis Is Essential for Survival of Leishmania Infantum.” MBio, vol. 8, no. 1, 2017, doi : 10.1128/mbio.01121-16
  10. ↑ Macedo-Silva, Virgínia P.; Martins, Daniella R. A.; De Queiroz, Paula Vivianne Souza; Pinheiro, Marcos Paulo G.; Freire, Caio C. M.; Queiroz, José W.; Dupnik, Kathryn M.; Pearson, Richard D.; Wilson, Mary E.; Jeronimo, Selma M. B.; Ximenes, Maria De Fátima F.M. (1 January 2014). "Feeding Preferences of Lutzomyia longipalpis (Diptera: Psychodidae), the Sand Fly Vector, for Leishmania infantum (Kinetoplastida: Trypanosomatidae)". Journal of Medical Entomology. 51 (1): 237–244. doi:10.1603/me12131. PMC   4277188 . PMID   24605474.
  11. 1 2 3 Graça-Souza, C. Maya-Monteiro, G. O. Paiva-Silva et al., “Adaptations against heme toxicity in blood-feeding arthropods,” Insect Biochemistry and Molecular Biology, vol. 36, no. 4, pp. 322–335, 2006.
  12. 1 2 3 4 5 6 7 Alexander, Bruce; Lopes de Carvalho, Renata; McCallum, Hamish; Pereira, Marcos Horácio (December 2002). "Role of the Domestic Chicken (Gallus gallus)in the Epidemiology of Urban Visceral Leishmaniasis in Brazil". Emerging Infectious Diseases. 8 (12): 1480–1485. doi:10.3201/eid0812.010485. PMC   2738513 . PMID   12498667.
  13. 1 2 Abbehusen, Melissa Moura Costa, et al. “Immunization of Experimental Dogs With Salivary Proteins From Lutzomyia Longipalpis, Using DNA and Recombinant Canarypox Virus Induces Immune Responses Consistent With Protection Against Leishmania Infantum.” Frontiers in Immunology, vol. 9, 2018, doi : 10.3389/fimmu.2018.02558
  14. ↑ Carrasquilla, María C. “Featured Creatures: Lutzomyia Longipalpis.” Entomology and Nematology Department, University of Florida, University of Florida, May 2015, entnemdept.ufl.edu/creatures/misc/flies/Lutzomyia_longipalpis.htm.
  15. 1 2 Casanova, Cláudio; Andrighetti, Maria T. M.; Sampaio, Susy M. P.; Marcoris, Maria L. G.; Colla-Jacques, Fernanda E.; Prado, Ângelo P. (2013-09-19). "Larval Breeding Sites of Lutzomyia longipalpis (Diptera: Psychodidae) in Visceral Leishmaniasis Endemic Urban Areas in Southeastern Brazil". PLOS Neglected Tropical Diseases. 7 (9): e2443. doi: 10.1371/journal.pntd.0002443 . ISSN   1935-2735. PMC   3777886 . PMID   24069494.
  16. 1 2 N. F. C. Secundino, I. Eger-Mangrich, E. M. Braga, M. M. Santoro, and P. F. P. Pimenta, “Lutzomyia longipalpis peritrophic matrix: Formation, structure, and chemical composition,” Journal of Medical Entomology, vol. 42, no. 6, pp. 928–938, 2005.
  17. ↑ R. S. Milleron, C. R. Meneses, D. A. Elnaiem, and G. C. Lanzaro, “Effects of varying moisture on egg production and longevity of Lutzomyia longipalpis (Diptera: Psychodidae),” Journal of Medical Entomology, vol. 45, no. 1, pp. 160–165, 2008.
  18. ↑ MD. Buescher, LC. Rutledge, J. Roberts, and JH. Nelson, Observations on multiple feeding by Lutzomyia longipalpis in the laboratory (Diptera: Psychodidae), Mosquito News, 1984.
  19. ↑ Morton, IE; Ward, RD (July 1989). "Laboratory response of female Lutzomyia longipalpis sandflies to a host and male pheromone source over distance". Medical and Veterinary Entomology. 3 (3): 219–23. doi:10.1111/j.1365-2915.1989.tb00218.x. PMID   2519666. S2CID   22550221.
  20. ↑ Michalsky, Érika Monteiro; Fortes-Dias, Consuelo Latorre; França-Silva, João Carlos; Rocha, Marilia Fonseca; Barata, Ricardo Andrade; Dias, Edelberto Santos (December 2009). "Association of Lutzomyia longipalpis (Diptera: Psychodidae) population density with climate variables in Montes Claros, an area of American visceral leishmaniasis transmission in the state of Minas Gerais, Brazil". Memórias do Instituto Oswaldo Cruz. 104 (8): 1191–1193. doi: 10.1590/S0074-02762009000800020 . hdl: 1807/58031 . PMID   20140384.
  21. ↑ Costa, F. V., Siqueira Neves, F., Oliveira Silva, J. & Fagundes, M. Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod-Plant Interactions5, 9–18 (2010).
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.